Learning-dependent plasticity of hippocampal CA1 pyramidal neuron postburst afterhyperpolarizations and increased excitability after inhibitory avoidance learning depend upon basolateral amygdala inputs

Hippocampus

Volumn 22, Issue 8, 2012, Pages 1703-1719

  Farmer, George E ^a   Thompson, Lucien T ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Acquisition; Consolidation; Inactivation; Postburst AHP; Single trial learning

Indexed keywords

BUPIVACAINE; LIDOCAINE;

ACCOMMODATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BASOLATERAL AMYGDALA; CELL POLARITY; CELL POPULATION; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; MALE; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; TASK PERFORMANCE;

ACTION POTENTIALS; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BLINKING; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CONDITIONING, CLASSICAL; MALE; NEURONAL PLASTICITY; PYRAMIDAL CELLS; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 84863775822     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22005     Document Type: Article

References (56)

1. Aicardi G, Schwartzkroin PA. 1990. Suppression of epileptiform burst discharges in CA3 neurons of rat hippocampal slices by the organic calcium channel blocker, verapamil. Exp Brain Res 81: 288-296.
2. Ammassari-Teule M, Pavone F, Castellano C, McGaugh JL. 1991. Amygdala and dorsal hippocampus lesions block the effects of GABAergic drugs on memory storage. Brain Res 551: 104-109.
3. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN. 1999. Double dissociation of function within the hippocampus: A comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113: 1170-1188.
4. Bannerman DM, Deacon RM, Offen S, Friswell J, Grubb M, Rawlins JN. 2002. Double dissociation of function within the hippocampus: Spatial memory and hyponeophagia. Behav Neurosci 116: 884-901.
5. Barkai E, Saar D. 2001. Cellular correlates of olfactory learning in the rat piriform cortex. Rev Neurosci 12: 111-120.
6. Chen C, Kim JJ, Thompson RF, Tonegawa S. 1996. Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behav Neurosci 110: 1177-1180.
7. De Boer SF, Slangen JL, Van der Gugten J. 1990. Plasma catecholamine and corticosterone levels during active and passive shock-prod avoidance behavior in rats: Effects of chlordiazepoxide. Physiol Behav 47: 1089-1098.
8. Disterhoft JF, Coulter DA, Alkon DL. 1986. Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci USA 83: 2733-2737.
9. Dutar P, Nicoll RA. 1989. Pharmacological characterization of muscarinic responses in rat hippocampal pyramidal cells. Exs 57: 68-76.
10. Gant JC, Thompson LT. 2000. Calmodulin mediated plasticity in rat CA1 neurons following spatial learning. Soc Neurosci Abstr 30, 73.11.
11. Gu N, Vervaeke K, Hu H, Storm JF. 2005. Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566 (Part 3): 689-715.
12. Gustafsson B, Wigstrom H. 1981. Evidence for two types of afterhyperpolarization in CA1 pyramidal cells in the hippocampus. Brain Res 206: 462-468.
13. Haas HL, Greene RW. 1984. Adenosine enhances afterhyperpolarization and accommodation in hippocampal pyramidal cells. Pflugers Arch 402: 244-247.
14. Hennevin E, Maho C, Hars B. 1998. Neuronal plasticity induced by fear conditioning is expressed during paradoxical sleep: Evidence from simultaneous recordings in the lateral amygdala and the medial geniculate in rats. Behav Neurosci 112: 839-862.
15. Hotson JR, Prince DA. 1980. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J Neurophysiol 43: 409-419.
16. Hui GK, Figueroa IR, Poytress BS, Roozendaal B, McGaugh JL, Weinberger NM. 2004. Memory enhancement of classical fear conditioning by posttraining injections of corticosterone in rats. Neurobiol Learn Mem 81: 67-74.
17. Izquierdo I, Medina JH. 1993. Role of the amygdala, hippocampus and entorhinal cortex in memory consolidation and expression. Braz J Med Biol Res 26: 573-589.
18. Kim JJ, Clark RE, Thompson RF. 1995. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109: 195-203.
19. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB. 2002. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99: 10825-10830.
20. Lancaster B, Hu H, Gibb B, Storm JF. 2006. Kinetics of ion channel modulation by cAMP in rat hippocampal neurones. J Physiol 576 (Part 2): 403-417.
21. Liang KC, McGaugh JL, Martinez JLJr, Jensen RA, Vasquez BJ, Messing RB. 1982. Posttraining amygdaloid lesions impair retention of an inhibitory avoidance response. Behav Brain Res 4: 237-249.
22. Madison DV, Nicoll RA. 1982. Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299: 636-638.
23. Madison DV, Nicoll RA. 1984. Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol 354: 319-331.
24. Madison DV, Nicoll RA. 1986. Actions of noradrenaline recorded intracellularly in rat hippocampal CA1 pyramidal neurones, in vitro. J Physiol 372: 221-244.
25. Matthews EA, Linardakis JM, Disterhoft JF. 2009. The fast and slow afterhyperpolarizations are differentially modulated in hippocampal neurons by aging and learning. J Neurosci 29: 4750-4755.
26. McGaugh JL, McIntyre CK, Power AE. 2002. Amygdala modulation of memory consolidation: Interaction with other brain systems. Neurobiol Learn Mem 78: 539-552.
27. McIntyre CK, Power AE, Roozendaal B, McGaugh JL. 2003a. Role of the basolateral amygdala in memory consolidation. Ann N Y Acad Sci 985: 273-293.
28. McIntyre CK, Power AE, Roozendaal B, McGaugh JL. 2003b. Role of the basolateral amygdala in memory consolidation. Ann N Y Acad Sci 985: 273-293.
29. McIntyre CK, Miyashita T, Setlow B, Marjon KD, Steward O, Guzowski JF, McGaugh JL. 2005. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proc Natl Acad Sci USA 102: 10718-10723.
30. McKernan MG, Shinnick-Gallagher P. 1997. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390: 607-611.
31. Miranda MI, LaLumiere RT, Buen TV, Bermudez-Rattoni F, McGaugh JL. 2003. Blockade of noradrenergic receptors in the basolateral amygdala impairs taste memory. Eur J Neurosci 18: 2605-2610.
32. Moyer JRJr, Thompson LT, Disterhoft JF. 1996. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 16: 5536-5546.
33. Moyer JRJr, Power JM, Thompson LT, Disterhoft JF. 2000. Increased excitability of aged rabbit CA1 neurons after trace eyeblink conditioning. J Neurosci 20: 5476-5482.
34. Oh MM, Kuo AG, Wu WW, Sametsky EA, Disterhoft JF. 2003. Watermaze learning enhances excitability of CA1 pyramidal neurons. J Neurophysiol 90: 2171-2179.
35. Oh MM, McKay BM, Power JM, Disterhoft JF. 2009. Learning-related postburst afterhyperpolarization reduction in CA1 pyramidal neurons is mediated by protein kinase A. Proc Natl Acad Sci USA 106: 1620-1625.
36. Ottersen OP. 1982. Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J Comp Neurol 205: 30-48.
37. Pare D. 2003. Role of the basolateral amygdala in memory consolidation. Prog Neurobiol 70: 409-420.
38. Parent MB, McGaugh JL. 1994. Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training. Brain Res 661: 97-103.
39. Pedarzani P, Storm JF. 1993. PKA mediates the effects of monoamine transmitters on the K+ current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11: 1023-1035.
40. Pedarzani P, Storm JF. 1995. Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons. J Neurophysiol 74: 2749-2753.
41. Petrovich GD, Risold PY, Swanson LW. 1996. Organization of projections from the basomedial nucleus of the amygdala: A PHAL study in the rat. J Comp Neurol 374: 387-420.
42. Pikkarainen M, Ronkko S, Savander V, Insausti R, Pitkanen A. 1999. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol 403: 229-260.
43. Pothuizen HH, Zhang WN, Jongen-Relo AL, Feldon J, Yee BK. 2004. Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: A within-subject, within-task comparison of reference and working spatial memory. Eur J Neurosci 19: 705-712.
44. Quirarte GL, Roozendaal B, McGaugh JL. 1997. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci USA 94: 14048-14053.
45. Roozendaal B, McReynolds JR, Van der Zee EA, Lee S, McGaugh JL, McIntyre CK. 2009. Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala. J Neurosci 29: 14299-14308.
46. Saar D, Grossman Y, Barkai E. 1998. Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur J Neurosci 10: 1518-1523.
47. Schenberg EE, Soares JC, Oliveira MG. 2005. Effects of pre- or posttraining entorhinal cortex AP5 injection on fear conditioning. Physiol Behav 86: 508-515.
48. Schwartzkroin PA. 1975. Characteristics of CA1 neurons recorded intracellularly in the hippocampal in vitro slice preparation. Brain Res 85: 423-436.
49. Schwartzkroin PA, Stafstrom CE. 1980. Effects of EGTA on the calcium-activated afterhyperpolarization in hippocampal CA3 pyramidal cells. Science 210: 1125-1126.
50. Silva MA, Tomaz C. 1995. Amnesia after diazepam infusion into basolateral but not central amygdala of Rattus norvegicus. Neuropsychobiology 32: 31-36.
51. Staubli U, Ivy G, Lynch G. 1984. Hippocampal denervation causes rapid forgetting of olfactory information in rats. Proc Natl Acad Sci USA 81: 5885-5887.
52. Storm JF. 1989. An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J Physiol 409: 171-190.
53. Thompson LT, Gant JC, Lea P. 2000. Postsynaptic plasticity in young and aging rat CA1 neurons and spatial learning: Further emphasis on accommodation. Soc Neurosci Abstr 30, 73.12.
54. Thompson LT, Moyer JRJr, Disterhoft JF. 1996. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J Neurophysiol 76: 1836-1849.
55. Vazdarjanova A, McGaugh JL. 1999. Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. J Neurosci 19: 6615-6622.
56. Zelcer I, Cohen H, Richter-Levin G, Lebiosn T, Grossberger T, Barkai E. 2006. A cellular correlate of learning-induced metaplasticity in the hippocampus. Cereb Cortex 16: 460-468.